The Plant Vascular System: Evolution, Development and FunctionsF

are beginning to reveal important mechanisms in how the
balance of cell differentiation and cell division is regulated, and
how tissue identity is maintained across layers of secondary
vascular tissues. Recent studies in Arabidopsis and Populus
have identified mechanisms by which the balance of cell differentiation
and tissue identity are established through cell-cell
signaling. As previously discussed, in Arabidopsis, TDIFisa
small peptide product of the phloem-expressed CLE41/44 gene
(Ito et al. 2006). TDIF is secreted from the phloem, and acts to
inhibit tracheary element differentiation and stimulate cambial
activity (Ito et al. 2006; Hirakawa et al. 2008; Etchells and
Turner 2010), as well as to regulate the orientation of cambial
divisions (Etchells and Turner 2010). This peptide is perceived
by the LRR-Receptor kinase Phloem Intercalated with Xylem
(PXY), which is expressed in the procambium (Hirakawa et al.
2008; Hirakawa et al. 2010). Loss-of-function pxy mutants
show phloem cells intermixed in the xylem (Fisher and Turner
2007). TRIF/PXY signaling activates WOX4 (Hirakawa et al.
2010), which encodes a transcription factor that presumably
influences gene expression associated with meristematic cell
fate. Interestingly, stimulation of cambial activity by auxin
requires functional WOX4 and PXY (Suer et al. 2011), providing
insight into how auxin integrates into transcriptional regulation
in secondary vascular tissues.
Patterning and polarity in secondary vascular tissues
Cross sections of a typical woody stem show that secondary
vascular tissues are highly patterned (Figure 12), and that the
proper position and patterning of the cambium, secondary
xylem, and secondary phloem are crucial to the function of
these tissues. Additionally, secondary vascular tissues can
be described in terms of polarity, analogous to vasculature in
leaves. Take for example the vasculature of a typical dicot tree,
poplar, in which the vascular bundles in leaves always have
xylem towards the adaxial and phloem towards the abaxial
surface of the leaf. By following those vascular bundles through
the leaf trace and into the stem, it becomes apparent that
the same polarity relationships are found in both primary and
secondary vascular tissues, with xylem towards the center and
phloem towards the outside of the stem.
Insights into how polarity is established and maintained
in vascular tissues has been provided by pioneering studies
of the Class III HD-ZIP and KANADI transcription factors in
Arabidopsis. These Class III HD-ZIPs are highly conserved
in plants, act antagonistically with KANADIs, and have been
shown to regulate fundamental aspects of meristem function,
polarity, and vascular development (Emery et al. 2003; Izhaki
and Bowman 2007; Bowman and Floyd 2008). In Arabidopsis,
REV is implicated in various developmental processes,
including patterning of primary vascular bundles (Emery et al.
2003; Bowman and Floyd 2008). A recent study showed that
Insights into Plant Vascular Biology 321
misexpression of a Populus REV ortholog results in formation
of ectopic cambia in the cortex of the stem, and that these
cambia can produce secondary xylem with reversed polarity
(Robischon et al. 2011), indicating that the Class III HD-ZIPs
also affect patterning and polarity in secondary vasculature.
Genetics and genomics: critical tools for advancing
knowledge on woody growth
Research on secondary growth is at an exciting point, as genomic
tools are now allowing the characterization of the genetic
variation within species that is responsible for wood quality and
growth traits. Association mapping is being taken to a wholegenome
scale for some tree species, and will undoubtedly
provide fascinating insights into macro- and micro-evolution
of wood formation (Neale and Kremer 2011). Genomic tools
are also now enabling the first generation of network biology
approaches in the model tree genus Populus (Street et al.
2011) that can be used in understanding woody growth. Such
approaches utilize a variety of genomic data types to model
the genetic networks that regulate specific aspects of woody
growth, and can ultimately produce a “wiring diagram” of regulatory
networks. This will be important for both better directing
future research and for providing predictive models that can
potentially be used to better direct breeding programs, identify
regulatory genes for biotechnology, and provide insights into
the complexities of biological processes fundamental to the
future of forests worldwide.
Physical and Physiological Constraints
on Phloem Transport Function
We now turn our attention to an examination of the constraints
of photoassimilate transport in the most evolutionarily
advanced plants, the angiosperms. Here, photoassimilate
conducting units are comprised of SEs arranged end-to-end to
form conduits that are referred to as sieve tubes. At maturity,
SEs lack nuclei and vacuoles, and their parietal cytoplasm
has a greatly reduced number of organelles. In contrast to
xylem tracheary elements, SEs retain their semi-permeable
plasma membrane. Their shared end walls contain interconnecting
pores (sieve plate pores) formed from PD coalescing
within pit fields (Evert 2006). In addition, each SE is highly
interconnected symplasmically with a metabolically active CC,
through specialized PD, to form a functional unit referred to as
the SE-CC complex.
In order to provide a framework on which to identify the
physical and physiological constraints regulating phloem transport,
we must first examine the physical mechanisms responsible
for resource transport through the sieve tube system.
As photoassimilate flow is polarized from source leaves (net
exporters of resources) to heterotrophic sinks (net importers